VENUS 76 (1–4): 39–44, 2018 First Cuspidariid Associated with Hydrothermal Vent 39 ©The Malacological Society of Japan DOI: http://doi.org/10.18941/venus.76.1-4_39
The First Cuspidariid Bivalve Associated with a Hydrothermal Vent Discovered from the Southern Mariana Trough Chong Chen1*, Takashi Okutani2, Hiromi Kayama Watanabe1 and Shigeaki Kojima3 1
Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa 237-0061, Japan 2 4-17-1-714 Takaishi, Asao-ku, Kawasaki, Kanagawa 215-0003, Japan 3 Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
Abstract: Cuspidariidae is a family of bizarre heterodont bivalves with a specialized carnivorous lifestyle. An unusual cuspidariid bivalve was discovered from 2,489 m depth in the Snail hydrothermal vent site, Southern Mariana Trough, and is described herein as Thermomya sulcata n. gen. & n. sp. Although cuspidariids are well-known from the deep sea, until now none were known to inhabit chemosynthetic ecosystems. In fact, this is also the first member of the clade Anomalodesmata found in hydrothermal vent ecosystems. Keywords: Anomalodesmata, new genus, new species, vent, Southern Mariana Trough
Introduction A diverse range of bivalve mollusks have been reported from animal communities associated with thermal vents or cold seeps. However, such vent/seep associated bivalves have hitherto been limited to a few families, mainly Solemyidae, Mytilidae (Bathymodiolus etc.), Lucinidae, Thyasiridae, and Vesicomyidae (Calyptogena etc.) (Sasaki et al., 2005; Desbruyères et al., 2006; Kiel, 2010; Taylor & Glover, 2010; Roeselers & Newton, 2012). Among biological samples collected by DSV Shinkai 6500 Dive 1228 (Southern Mariana Trough, 2,849 m depth), two small bivalve specimens apparently belonging to the family Cuspidariidae were collected. Subsequent morphological investigations validated this, thus confirming the discovery of the first cuspidariids from chemosynthetic ecosystems. Cuspidariidae is a family containing approximately 260 species (Machado et al., 2017) of strictly carnivorous heterodont bivalves characterized by shells with a conspicuous posterior rostrum, currently placed within the clade Anomalodesmata in the basal Imparidentia (Bieler et al., 2014). Although cuspidariids mostly occur at deep and often abyssal depths, none have been recovered from chemosynthetic ecosystems until the present discovery, which is also the first report of a living bivalve from the clade Anomalodesmata associated with hydrothermal vent ecosystems (see Kiel et al., 2010 for fossil species in order Modiomorphoida, which may be anomalodesmatans). The two individuals collected belonged to a hitherto undescribed species, which is so unusual that it cannot be assigned to any existing genus and thus a new genus is herein described. Abbreviations: JAMSTEC – Japan Agency for Marine-Earth Science and Technology, Yokosuka; NSMT – National Museum of Nature and Science, Tsukuba; SH – shell height; SL – shell length; SW – shell width. * Corresponding author:
[email protected] http://zoobank.org/urn:lsid:zoobank.org:pub:48EC52F5-1604-48B7-A69A-3C59D738E58D
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Taxonomy Subclass Heterodonta Neumayr, 1884 Superorder Anomalodesmata Dall, 1889 Superfamily Cuspidarioidea Dall, 1886 Family Cuspidariidae Dall, 1886
Thermomya n. gen. Type species: Thermomya sulcata n. sp., by monotypy. Diagnosis: Cuspidariid with short rostrum and evenly spaced, sharply edged, raised commarginal ribs on shell disc. Rostrum short, abruptly laterally compressed, without commarginal ribs but with irregular growth lines. Hinge plate weak and nearly straight. Ligament external, weak, and parivincular. Shell surface with wrinkled microsculpture, shell spicules lacking. Likely associated with thermal vent habitats. The gender is feminine. Etymology: From ‘Thermós’ (Greek), warm or hot, referring to its hot vent habitat in combination with ‘Myax’ (Greek), sea-mussel. Remarks: Commarginal ribs are common on several species of the related genus Cuspidaria Nardo, 1840, e.g., C. nobilis (Adams, 1864), C. ascoldica Scarlato, 1972 and C. okezoko Okutani, 1985, but such ribs in Cuspidaria species are usually rounded, unlike those in the present new genus which are sharply raised. Within the genus Myonera Dall, 1886, some species such as M. dispar (Dall, Bartsch & Rehder, 1938) and M. rostra Poutiers & Bernard, 1995 possess commarginal ribs. However, the commarginal ribs seen in genus Myonera are rounded and not sharply raised. Furthermore, this genus is characterized in having a vertical resilifer, unlike the present new genus. Members of the genus Bathyneaera Scarlato & Starobogatov, 1983, typified by Bathyneaera hadalis (Knudsen, 1970), also exhibit commarginal ribs, but the ribs seen in this genus are also rounded and are further crossed by radial riblets. The posterior rostrum of Bathynearea differs from Thermomya n. gen. in being alate and not demarcated from the disc.
Thermomya sulcata n. sp. (Figs 1–2) Description: Shell (Fig. 1) fragile, thin, opaque, longitudinally subquadrate in profile, subequilateral. Shell length 1.6 times greater than height and 2.4 times longer than width, inequivalve: right valve slightly larger and deeper than left. Beaks narrow, slightly prosogyrate, situated at midpoint of anterior-posterior axis. Antero-dorsal, anterior and ventral margins smooth, rounded in outline, but angulate at postero-ventral corner, at end of blunt radial ridge running from umbo to that point, demarcating shell disc and short posterior rostrum. Rostrum abruptly laterally compressed posterior of aforementioned ridge. Another much lower radial ridge runs from umbo to posterior margin. Rostrum strongly compressed between these two ridges to generate shallow sinus on ventral margin. Ligament external, weak, parivincular. Profile of rostrum trapezoidial due to posterior margin being nearly truncate. Surface of disc ornamented by widely spaced, sharp-edged, weakly upturned, raised commarginal ribs. Commarginal ribs seldom intercalated by secondary riblets, instead only weak growth lines present between ribs. On rostrum these ribs become abruptly disarrayed, almost vanishing, replaced by rather rough, irregular growth lines, intercalated by discontinuous, short, irregular shaped cords. Shell microsculpture (Fig. 2) consisting of wavy wrinkles; shell spicules lacking.
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Fig. 1. Thermomya sulcata n. gen. & n. sp. A–F. Holotype, NSMT-Mo 78997; left external (A), right external (B), right internal (C), left internal (D), dorsal view (E), hinge details (F). G–H. Paratype, NSMT-Mo 78998, left external (G), right external (H).
Fig. 2. Thermomya sulcata n. gen. & n. sp., shell microsculpture of the paratype (NSMT-Mo 78998) observed using scanning electron microscopy after cleaning with diluted bleach and removing the periostracum. A. Overview of intercostal space between commarginal ribs (posterior half of the left valve). B. Close-up. Scale bars: A = 100 µm; B = 10 μm.
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Inner surface dull white, with sign of commarginal grooves on disc reflecting surface sculpture. Adductor and pallial scars indistinct. Hinge plate weak, nearly straight. Left valve edentulous with rather thick nymphal ridge and oblique resilifer. Right valve also edentulous with resilifer below beak. Nymphal ridge not developed. Inner surface of rostrum flat. Type material: Holotype, NSMT-Mo 78997, a single conjoined specimen, SL 8.1 mm, SH 4.9 mm, SW 3.6 mm; paratype, NSMT-Mo 78998, a single conjoined, fractured specimen preserved in ethanol, SL ca. 5.5 mm, SH ca. 3.6 mm. All collected from the type locality. Type Locality: Snail site, Southern Mariana Trough, 12°57.189´N, 143°37.166´E, 2,849 m depth (Fig. 3). DSV Shinkai 6500 Dive #1228; September 14, 2010, Scientist on-board HOV: Shigeaki Kojima. R/V Yokosuka cruise YK10-11 (Principal Investigator: Shigeaki Kojima). Recovered from washings fixed and stored in 99% ethanol. Etymology: From Latin ‘sulcatus’, meaning having deep grooves or furrows, referring to its characteristic sculpture. Remarks: Commarginal ribs, which are sharply-edged, slightly upturned and well spaced, resembling those of some species of Placamen (Veneridae), are the key characters. For comparisons with other cuspidariids that also exhibit commarginal ribs, see Remarks section under the description of Thermomya n. gen. It is only known from the type locality. All described confamilial taxa are unknown from not only vents but also chemosynthetic ecosystems in general.
Discussion Thermomya sulcata n. gen. & n. sp. is the first cuspidariid bivalve known to be associated with a hydrothermal vent or any chemosynthetic ecosystems (Taylor & Glover, 2010; Amano, 2014), despite their being generally common in deep-sea muddy habitats and characteristic of the deep-sea biota (Knudsen, 1970; Knudsen, 1979). The absence of members of the superorder Anomalodesmata has been argued to be a prominent characteristic of deep-sea vents and seep communities (Sasaki et al., 2005), but the present discovery indicates that this is not the case. Due to the difficulty in sampling infaunal molluscs in hydrothermal vents (as they are not immediately visible), their diversity has undoubtedly been underestimated to date. It will be of great interest to 30˚N
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see if further cuspidariid species inhabiting vents or seeps will be found in the future. The soft parts of both specimens available were unfortunately not preserved in good condition, probably due to poor penetration of ethanol in the bulk-fixed washing sample. Despite many attempts, no DNA barcode sequences could be obtained from either specimen. Similarly, no anatomical details could be retrieved for this reason. The associated molluscs found in the immediate surroundings where the present new species was collected are the gastropods Provanna nassariaeformis Okutani, 1990, Desbruyeresia marianaenis (Okutani & Fujikura, 1990), Pachydermia sculpta Warén & Bouchet, 1993, Phymorhynchus aff. starmeri Okutani & Ohta, 1993, Shinkailepas aff. kaikatensis Okutani, Saito & Hashimoto, 1989, Ventsia aff. tricarinata Warén & Bouchet, 1993 (all sensu Warén & Bouchet, 2001), and Lepetodrilus aff. schrolli Beck, 1993 (sensu Johnson et al., 2008). All these gastropods are considered to be endemic to hydrothermal vent ecosystems (Okutani, 1990; Warén & Bouchet, 2001; Kojima & Watanabe, 2015).
Acknowledgements The authors gratefully acknowledge the tireless effort and support of the captain and crew of R/V Yokosuka as well as the pilots and technical team of DSV Shinkai 6500 during the research cruise YK10-11. Dr. Miho Asada (JAMSTEC) is sincerely thanked for her help in generating the bathymetric map used herein. Two anonymous reviewers are thanked for improving an earlier version of the manuscript.
References Amano, K. 2014. Fossil records and evolution of chemosynthetic bivalves. Fossils 96: 5–14. (in Japanese with English abstract) Bieler, R., Mikkelsen, P. M., Collins, T. M., Glover, E. A., González, V. L., Graf, D. L., Harper, E. M., Healy, J., Kawauchi, G. Y., Sharma, P. P., Staubach, S., Strong, E. E., Taylor, J. D., Tëmkin, I., Zardus, J. D., Clark, S., Guzmán, A., McIntyre, E., Sharp, P. & Giribet, G. 2014. Investigating the Bivalve Tree of Life – an exemplar-based approach combining molecular and novel morphological characters. Invertebrate Systematics 28: 32–115. Desbruyères, D., Segonzac, M. & Bright, M. 2006. Handbook of Deep-Sea Hydrothermal Vent Fauna (Second completely revised edition). Denisia 18: 1–544. Johnson, S. B., Warén, A. & Vrijenhoek, R. C. 2008. DNA barcoding of Lepetodrilus limpets reveals cryptic species. Journal of Shellfish Research 27: 43–51. Kiel, S. 2010. The fossil record of vent and seep mollusks. In: Kiel, S. (ed.), The Vent and Seep Biota: Aspects from Microbes and Ecosystems, pp. 255–277. Springer, Dordrecht, Heidelberg, London and New York. Knudsen, J. 1970. The systematics and biology of abyssal and hadal Bivalvia. Galathea Report 11: 5–241. Knudsen, K. 1979. Deep-sea bivalves. In: van der Spoel, S., van Bruggen, A. C. & Lever, J. (eds), Pathways in Malacology, pp. 195–224. Scheltema & Holkema, Utrecht, Netherlands. Kojima, S. & Watanabe, H. 2015. Vent fauna in the Mariana Trough. In: Ishibashi, J.-i., Okino, K. & Sunamura, M. (eds), Subseafloor Biosphere Linked to Hydrothermal Systems: TAIGA Concept, pp. 313–323. Springer Japan, Tokyo. Machado, F., Morton, B. & Passos, F. 2017. Functional morphology of Cardiomya cleryana (d’Orbigny, 1842) (Bivalvia: Anomalodesmata: Cuspidariidae) from Brazilian waters: New insights into the lifestyle of carnivorous bivalves. Journal of the Marine Biological Association of the United Kingdom 97: 447–462. Okutani, T. 1990. Two new species of Provanna (Gastropoda: Cerithiacea) from “snail pit” in the hydrothermal vent site at the Mariana Back-Arc Basin. Venus (Japanese Journal of Malacology) 49: 19–24. Roeselers, G. & Newton, I. L. 2012. On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Applied Microbiology and Biotechnology 94: 1–10. Sasaki, T., Okutani, T. & Fujikura, K. 2005. Molluscs from hydrothermal vents and cold seeps in Japan: A review of taxa recorded in twenty recent years (1984–2004). Venus 64: 87–133. Taylor, J. D. & Glover, E. A. 2010. Chemosynthetic bivalves. In: Kiel, S. (ed.), The Vent and Seep Biota: Aspects from Microbes and Ecosystems, pp. 107–135. Springer, Dordrecht, Heidelberg, London and New York.
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Warén, A. & Bouchet, P. 2001. Gastropoda and Monoplacophora from hydrothermal vents and seeps: New taxa and records. The Veliger 44: 116–231. (Received September 27, 2017 / Accepted November 16, 2017)
南部マリアナトラフの熱水噴出孔付近から初めて発見されたシャクシガイ科二枚貝 陳 充・奥谷喬司・渡部裕美・小島茂明
要 約 「しんかい 6500」によって南マリアナ舟状海盆の熱水噴出孔付近，水深 2,489 m から発見された微小な シャクシガイ科の二枚貝は化学合成生物群集の中から発見された最初のシャクシガイ類であり，最初の異 靱帯類でもある。 Thermomya sulcata n. gen. & n. sp. ユメノシャクシガイ（新属・新種・新称） 殻長 8.1 mm（ホロタイプ）。殻はよく膨れ，右殻が左殻より僅かに大きく不等殻。 殻体部には同心円状の板状肋がほぼ等間隔に並ぶ。嘴部は短く，筒状にはならず偏圧された亜三角形の 翼状。嘴上では板状肋は退化し皺状の成長脈となり不規則な脈条が散在する。鉸板は無歯。左殻の歯丘滑 層は厚い。シャクシガイ類のなかにはオオシャクシガイやミジンシャクシやオケゾコシャクシのように輪 肋を持ったものがあるが，それらの輪状肋は何れも密で丸みを帯びており，本種のようなハナガイ類のそ れのような間隔の空いた板状肋とは形状を異にする。 このような特異な形態学的特徴から新属を創設した。
